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Hindawi Publishing Corporation Advances in Virology Volume 2011, Article ID 734690, 7 pages doi:10.1155/2011/734690 Research Article The Effects of Temperature and Relative Humidity on the Viability of the SARS Coronavirus K. H. Chan, J. S. Malik Peiris, S. Y. Lam, L. L. M. Poon, K. Y. Yuen, and W. H. Seto Department of Microbiology, The University of Hong Kong, Queen Mary Hospital, Pokfulam, Hong Kong Correspondence should be addressed to K. H. Chan, [email protected] Received 25 November 2010; Revised 31 July 2011; Accepted 31 July 2011 Academic Editor: Alain Kohl Copyright © 2011 K. H. Chan et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The main route of transmission of SARS CoV infection is presumed to be respiratory droplets. However the virus is also detectable in other body fluids and excreta. The stability of the virus at dierent temperatures and relative humidity on smooth surfaces were studied. The dried virus on smooth surfaces retained its viability for over 5 days at temperatures of 22–25 C and relative humidity of 40–50%, that is, typical air-conditioned environments. However, virus viability was rapidly lost (>3 log 10 ) at higher temperatures and higher relative humidity (e.g., 38 C, and relative humidity of >95%). The better stability of SARS coronavirus at low temperature and low humidity environment may facilitate its transmission in community in subtropical area (such as Hong Kong) during the spring and in air-conditioned environments. It may also explain why some Asian countries in tropical area (such as Malaysia, Indonesia or Thailand) with high temperature and high relative humidity environment did not have major community outbreaks of SARS. 1. Introduction Severe acute respiratory syndrome (SARS), was a new emerging disease associated with severe pneumonia and spread to involve over 30 countries in 5 continents in 2003. A novel coronavirus was identified as its cause [13]. SARS had a dramatic impact on health care services and economies of aected countries, and the overall mortality rate was estimated to be 9%, but rising to 50% in those aged 60 or above [4]. A notable feature of this disease was its predilection for transmission in the health care setting and to close family and social contacts. The disease is presumed to be spread by droplets, close direct or indirect contact, but the relative importance of these routes of transmission is presently unclear. A study showed that viral aerosol genera- tion by a patient with SARS was possible and therefore air- borne droplet transmission was a possible means of trans- mission [5]. However, the role of fomites and environmental contamination in transmission of infection is presently still unclear. An outbreak of disease aecting over 300 residents in high-rise apartment block (Amoy Gardens) in Hong Kong could not be explained by respiratory droplet transmission from infected patients [6]. Infectious virus is detectable in the faeces [7], and aerosolization of virus in contaminated faeces is believed to be the mode of transmission of this outbreak [8]. We and others have reported that infectivity of SARS CoV (SARS coronavirus) was lost after heating at 56 C for 15 minutes but that it was stable for at least 2 days following drying on plastic. It was completely inactivated by common fixatives used in laboratory [9, 10]. Another study showed that it was inactivated by ultraviolet light, alkaline (pH > 12), or acidic (pH < 3) conditions [11]. Human coronaviruses have been shown to survive in PBS or culture medium with 5–10% FCS for several days [1214] but they only survive a few hours after drying [13, 14]. There have been some studies reporting an association between the SARS outbreak, metrological factors, and air pollution [1517]. Thus, infor- mation on the survival of the SARS coronavirus (SCoV) in the environment at dierent temperature and humidity conditions is of significant interest to understanding virus transmission. A recent study using surrogate coronaviruses (transmissible gastroenteritis virus (TGEV) and mouse hepatitis virus (MHC)) has investigated the eect of air

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Page 1: TheEffectsofTemperatureandRelativeHumidityonthe ...downloads.hindawi.com/journals/av/2011/734690.pdf2 Advances in Virology Table 1: WHO SARS report—based on data as of the 31st December

Hindawi Publishing CorporationAdvances in VirologyVolume 2011, Article ID 734690, 7 pagesdoi:10.1155/2011/734690

Research Article

The Effects of Temperature and Relative Humidity on theViability of the SARS Coronavirus

K. H. Chan, J. S. Malik Peiris, S. Y. Lam, L. L. M. Poon, K. Y. Yuen, and W. H. Seto

Department of Microbiology, The University of Hong Kong, Queen Mary Hospital, Pokfulam, Hong Kong

Correspondence should be addressed to K. H. Chan, [email protected]

Received 25 November 2010; Revised 31 July 2011; Accepted 31 July 2011

Academic Editor: Alain Kohl

Copyright © 2011 K. H. Chan et al. This is an open access article distributed under the Creative Commons Attribution License,which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

The main route of transmission of SARS CoV infection is presumed to be respiratory droplets. However the virus is also detectablein other body fluids and excreta. The stability of the virus at different temperatures and relative humidity on smooth surfaceswere studied. The dried virus on smooth surfaces retained its viability for over 5 days at temperatures of 22–25◦C and relativehumidity of 40–50%, that is, typical air-conditioned environments. However, virus viability was rapidly lost (>3 log10) at highertemperatures and higher relative humidity (e.g., 38◦C, and relative humidity of >95%). The better stability of SARS coronavirus atlow temperature and low humidity environment may facilitate its transmission in community in subtropical area (such as HongKong) during the spring and in air-conditioned environments. It may also explain why some Asian countries in tropical area(such as Malaysia, Indonesia or Thailand) with high temperature and high relative humidity environment did not have majorcommunity outbreaks of SARS.

1. Introduction

Severe acute respiratory syndrome (SARS), was a newemerging disease associated with severe pneumonia andspread to involve over 30 countries in 5 continents in2003. A novel coronavirus was identified as its cause [1–3].SARS had a dramatic impact on health care services andeconomies of affected countries, and the overall mortalityrate was estimated to be 9%, but rising to 50% in those aged60 or above [4]. A notable feature of this disease was itspredilection for transmission in the health care setting andto close family and social contacts. The disease is presumedto be spread by droplets, close direct or indirect contact, butthe relative importance of these routes of transmission ispresently unclear. A study showed that viral aerosol genera-tion by a patient with SARS was possible and therefore air-borne droplet transmission was a possible means of trans-mission [5]. However, the role of fomites and environmentalcontamination in transmission of infection is presently stillunclear. An outbreak of disease affecting over 300 residentsin high-rise apartment block (Amoy Gardens) in Hong Kongcould not be explained by respiratory droplet transmission

from infected patients [6]. Infectious virus is detectable inthe faeces [7], and aerosolization of virus in contaminatedfaeces is believed to be the mode of transmission of thisoutbreak [8].

We and others have reported that infectivity of SARS CoV(SARS coronavirus) was lost after heating at 56◦C for 15minutes but that it was stable for at least 2 days followingdrying on plastic. It was completely inactivated by commonfixatives used in laboratory [9, 10]. Another study showedthat it was inactivated by ultraviolet light, alkaline (pH> 12),or acidic (pH< 3) conditions [11]. Human coronaviruseshave been shown to survive in PBS or culture medium with5–10% FCS for several days [12–14] but they only survivea few hours after drying [13, 14]. There have been somestudies reporting an association between the SARS outbreak,metrological factors, and air pollution [15–17]. Thus, infor-mation on the survival of the SARS coronavirus (SCoV)in the environment at different temperature and humidityconditions is of significant interest to understanding virustransmission. A recent study using surrogate coronaviruses(transmissible gastroenteritis virus (TGEV) and mousehepatitis virus (MHC)) has investigated the effect of air

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2 Advances in Virology

Table 1: WHO SARS report—based on data as of the 31st December 2003.

Areas Total Medan age Deaths Case fatality Ratio (%) No. of imported Cases (%) No. of HCW (%) First case Last case

China 5327 NKn 349 7 NA 1002 (19) Nov-02 Jun-03

Hong Kong 1755 40 299 17 NA 386 (22) Feb-03 May-03

Taiwan 346 42 37 11 21 (6) 68 (20) Feb-03 Jun-03

Singapore 238 35 33 14 8 (3) 97 (41) Feb-03 May-03

Viet Nam 63 43 5 8 1 (2) 36 (57) Feb-03 Apr-03

Indonesia 2 56 0 0 2 (100) 0 (0) Apr-03 Apr-03

Malaysia 5 30 2 40 5 (100) 0 (0) Mar-03 Apr-03

Thailand 9 42 2 22 9 (100) 1 (11) Mar-03 May-03

Philippines 14 41 2 14 7 (50) 4 (29) Feb-03 May-03

Total 8096 774 9.6 142 1706 (21)

temperature and relative humidity on coronavirus survivalon surface [18]. The survival effects of these environmentalfactors on SARS coronavirus remain unclear. In the presentstudy, we report the stability of the SARS coronavirus at dif-ferent temperatures and relative humidity.

2. Material and Methods

2.1. Virus Strain and Cell Line. The SARS CoV strain used inthis study is HKU39849. Foetal monkey kidney cells (FRhK-4) were cultured in minimal essential medium (MEM, Gibco,USA) with 10% foetal calf serum and penicillin streptomycin(Gibco, USA) at 37◦C in 5% CO2 and were used for growingstock virus and for titration of viral infectivity [1, 2].

2.2. Preparation of Stock Virus. Stock virus was harvestedwhen infection approximately 75% of the cell monolayerof a virus infected flask manifested cytopathic effect (CPE).Infected cells were subjected to one cycle of freeze and thawcentrifuged at 2000 rpm for 20 minutes to remove cell debrisand the culture supernatant was aliquoted and stored at−80◦C until use.

2.3. Determination of Tissue Culture Infectious Dose (50%)(TCID50). 96-well microtitre plates containing 100 μL ofconfluent FRhK-4 were infected with 100 μL of serial 10-fold of dilutions of stock virus in minimal essential mediumwith 1% FCS (maintenance medium) starting from 10−1 to108. Titrations were done in quadruplicate. Infected cellswere incubated for 4 days at 37◦C. Appearance of CPE wasrecorded daily. TCID50 was determined according to Reedand the Muench method [19].

2.4. Effect of Drying, Heat, and Relative Humidity. Tenmicrolitre of maintenance medium containing 107 TCID50

per mL of virus was placed in individual wells of a 24-well plastic plates and allowed to dry at room temperature(22∼25◦C) and relative humidity of 40–50% (i.e., conditionsprevailing in a typical air-conditioned room). One hundredmicrolitre of MM was used to resuspend the virus at 0 hr,3 hr, 7 hr, 11 hr, 13 hr, 24 hr, and up to 4 weeks and the resi-dual virus infectivity was titrated. Controls in closed screw

cap eppendorf tube were included each time and treatedsimilarly but without drying.

The experiment was repeated at different temperatures(38◦C, 33◦C, 28◦C) and relative humidities (>95%, 80∼89%)for 3 hr, 7 hr, 11 hr, 13 hr, and 24 hr. A nebulizer under acontrolled condition was used to generate high and relativelow humidity environment. All the experiments above wereconducted in duplicate and the residual viral infectivity wastitrated.

2.5. Infectivity Assay. The infectivity of residual virus wastitrated in quadruplicate on 96-well microtitre plates con-taining 100 μL of confluent FRhK-4 cells. 100 μL of serial 10-fold of dilutions of virus in maintenance medium startingfrom 10−1 to 108 was added into FRhK-4 cells. The infectedcells were incubated at 37◦C for 4 days. Appearance of CPEwas recorded daily. TCID50 was determined according to theReed and Muench method [19].

3. Results

Ten microlitre of 107 TCID50 per mL of virus was placedin individual wells of a 24-well plastic plate (representinga nonporous surface) and dried. The dried virus was thenincubated at different temperatures (38◦C, 33◦C, 28◦C) atdifferent relative humidity (>95%, 80∼89%) for 3 hr, 7 hr,11 hr, 13 hr, and 24 hr and the residual viral infectivitywas titrated. A similar experiment was conducted at roomtemperature and relative humidity of about 40–50% (air-conditioned room) for up to 4 weeks. Virus dried on plasticretained viability for up to 5 days at 22∼25◦C at relative hum-idity of 40∼50% with only 1 log10 loss of titre (Figure 1).After that virus infectivity is gradually lost ever time. Lossof virus infectivity in solution was generally similar to driedvirus under these environmental conditions. This indicatesthat SARS CoV is a stable virus that may potentially betransmitted by indirect contact or fomites, especially in air-conditioned environments.

High relative humidity (>95%) at comparatively lowtemperature (28◦C and 33◦C) did not affect the virus infecti-vity significantly (Figure 2(a)). High temperature (38◦C) at80–90% relative humidity led to a 0.25∼2 log10 loss of titre at24 hr (Figure 2(b)). However, if the dried virus was stored at

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Advances in Virology 3

28 d21 d13 d7 d5 d2 d 3 d24 h13 h11 h7 h3 h0

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Figure 1: Residual virus infectivity at 22–25◦C with relative humi-dity 40–50% (starting titre 105/10 μL) and at 33◦C or 38◦C with re-lative humidity >95%.

high temperature (38◦C) and high relative humidity (>95%),there was a further ∼1.5 log loss of titre for each time pointup to 24 hr (0.38∼3.38 log10) when compared with hightemperature (38◦C) at a lower relative humidity 80–90%(Figures 3(a)–3(c)).

4. Discussion

Viruses do not replicate outside living cell but infectiousvirus may persist on contaminated environmental surfacesand the duration of persistence of viable virus is affectedmarkedly by temperature and humidity. Contaminatedsurfaces are known to be significant vectors in the transmis-sion of infections in the hospital setting as well as the com-munity. The role of fomites in the transmission of RSVhas been clearly demonstrated [20]. Survival of viruses ona variety of fomites has been studied for influenza viruses,paramyxoviruses, poxviruses, and retroviruses [21]. The hu-man coronavirus associated with the common cold wasreported to remain viable only for 3 hours on environmentalsurfaces after drying, although it remains viable for manydays in liquid suspension [13]. Parainfluenza and RSVviruses were viable after drying on surfaces for 2 and 6 hours,respectively [20, 22]. In aerosolised form, human corona-virus 229E is generally less stable in high humidity [12]. Theenvironmental stability of SCoV was previously unknownand this information is clearly important for understandingthe mechanisms of transmission of this virus in a hospitaland community setting.

In the present study, we have demonstrated that SARSCoV can survive at least two weeks after drying at temper-ature and humidity conditions found in an air-conditionedenvironment. The virus is stable for 3 weeks at room tem-perature in a liquid environment but it is easily killed byheat at 56◦C for 15 minutes [9]. This indicates that SARSCoV is a stable virus that may potentially be transmitted byindirect contact or fomites. These results may indicate that

contaminated surfaces may play a major role in transmissionof infection in the hospital and the community.

Our studies indicate that SCoV is relatively more stablethan the human coronaviruses 229E or OC43 and some otherviral respiratory pathogens such as respiratory syncytialvirus. These findings suggest that, while direct droplettransmission is an important route of transmission [23],the role of fomites and environmental contamination invirus transmission may play a significant role in virustransmission. In particular, fomites may contribute to thecontinued transmission of infection in the nosocomialsetting that continues to occur in spite of the great attentionand stringent precautions taken to prevent droplet spread.In addition to droplet precautions, reenforcing contactprecautions and hand washing is called for.

Faecal contamination of SCoV coronavirus may thusbe an effective route of transmission of the disease. Theoutbreak in Amoy Garden in Hong Kong which affected over300 residents in a single-apartment block with thought tohave been transmitted by contaminated sewage. The stabilityof the virus on environmental surfaces and its presencein faeces indicates the potential that fecal contaminationof fresh-food production may pose a threat for virustransmission; especially in countries with poor sanitationand sewage disposal systems and that studies to address thispossibility are needed.

In this study, we showed that high temperature at highrelative humidity has a synergistic effect on inactivationof SARS CoV viability while lower temperatures and lowhumidity support prolonged survival of virus on contami-nated surfaces. The environmental conditions of countriessuch as Malaysia, Indonesia, and Thailand are thus notconducive to the prolonged survival of the virus. In countriessuch as Singapore and Hong Kong where there is a inten-sive use of air-conditioning, transmission largely occurredin well-air-conditioned environments such as hospitals orhotels. Further, a separate study has shown that during theepidemic, the risk of increased daily incidence of SARS was18.18-fold higher in days with a lower air temperature thanin days with a higher temperature in Hong Kong [24] andother regions [15–17]. Taken together, these observationsmay explain why some Asian countries in tropical area (withhigh temperature at high relative humidity) such as Malaysia,Indonesia, and Thailand did not have nosocomial outbreaksof SARS (Tables 1 and 2(a)–2(c)). It may also explain whySingapore, which is also in tropical area (Table 2(d)), hadmost of its SARS outbreaks in hospitals (air-conditionedenvironment). Interestingly, during the outbreak of SARS inGuangzhou, clinicians kept the windows of patient roomsopen and well ventilated and these may well have reducedvirus survival and this reduced nosocomial transmission.SARS CoV can retain its infectivity up to 2 weeks atlow temperature and low humidity environment, whichmight facilitate the virus transmission in community as inHong Kong which locates in subtropical area (Table 2(e)).Other environmental factors including wind velocity, dailysunlight, and air pressure, had shown to be associatedwith SARS epidemic, should also be considered [16, 17].The dynamics of SARS epidemic involves multiple factors

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4 Advances in Virology

24 hr13 hr11 hr7 hr3 hr

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Figure 2: Infectivity of SARS Coronavirus (105/10 μL) to different temperatures at (a) >95% relative humidity, (b) >80–89%.

24 hr13 hr11 hr7 hr3 hr

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Figure 3: Infectivity of SARS Coronavirus (starting titre 105/10 μL) at different relative humidity at (a) 38◦C, (b) 33◦C, and (c) 28◦C.

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Advances in Virology 5

Table 2: A summary of the meteorological data of 2005 in average weather conditions∗.

Month Average sunlight (hours)Temperature

Discomfort from heat and humidityRelative humidity

Min Max am pm(a) Kuala Lumpur, Malaysia

Jan 6 22 32 High 97 60Feb 7 22 33 High 97 60March 7 23 33 High 97 58April 6 23 33 High 97 63May 6 23 33 High 97 66June 7 22 33 High 96 63July 7 23 32 High 95 63Aug 6 23 32 High 96 62Sept 6 23 32 High 96 64Oct 5 23 32 High 96 65Nov 5 23 32 High 97 66Dec 5 22 32 High 97 61

(b) Jakarta, IndonesiaJan 5 23 29 High 95 75Feb 5 23 29 High 95 75March 6 23 30 High 94 73April 7 24 31 High 94 71May 7 24 31 High 94 69June 7 23 31 High 93 67July 7 23 31 High 92 64Aug 8 23 31 High 90 61Sept 8 23 31 High 90 62Oct 7 23 31 High 90 64Nov 6 23 30 High 92 68Dec 5 23 29 High 92 71

(c) Bangkok, ThailandJan 9 20 32 High 91 53Feb 8 22 33 High 92 55March 9 24 34 High 92 56April 8 25 35 Extreme 90 58May 8 25 34 Extreme 91 64June 6 24 33 Extreme 90 67July 5 24 32 High 91 66Aug 5 24 32 High 92 66Sept 5 24 32 High 94 70Oct 6 24 31 High 93 70Nov 8 22 31 High 92 65Dec 9 20 31 High 91 56

(d) SingaporeJan 5 23 30 High 82 78Feb 7 23 31 High 77 71March 6 24 31 High 76 70April 6 24 31 High 77 74May 6 24 32 Extreme 79 73June 6 24 31 High 79 73July 6 24 31 High 79 72Aug 6 24 31 High 78 72Sept 5 24 31 High 79 72Oct 5 23 31 High 78 72Nov 5 23 31 High 79 75Dec 4 23 31 High 82 78

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6 Advances in Virology

Table 2: Continued.

Month Average sunlight (hours)Temperature

Discomfort from heat and humidityRelative humidity

Min Max am pm(e) Hong Kong

Jan 5 13 18 — 77 66Feb 4 13 17 — 82 73March 3 16 19 — 84 74April 4 19 24 Medium 87 77May 5 23 28 Medium 87 78June 5 26 29 High 86 77July 8 26 31 High 87 77Aug 6 26 31 High 87 77Sept 6 25 29 High 83 72Oct 7 23 27 Medium 75 63Nov 7 18 23 Moderate 73 60Dec 6 15 20 — 74 63∗

Data is available at BBC weather website (http://www.bbc.co.uk/weather/world/city guides/results).

including physical property of virus, outdoor and indoorenvironments, hygiene, space, and genetic predispositions[10, 15–17, 24, 25]. Understanding the stability of viruses indifferent temperature and humidity conditions is importantin understanding transmission of novel infectious agent in-cluding that of the recent influenza Apandemic H1N12009.

Conflict of Interests

The authors declare that there is no conflict of interest.

References

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Advances in Virology 7

[19] L. J. Reed and H. Muench, “A simple method of estimating fiftyper cent endpoints,” American Journal of Epidemiology, vol. 27,no. 3, pp. 493–497, 1938.

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ArchaeaHindawi Publishing Corporationhttp://www.hindawi.com Volume 2014

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Genetics Research International

Hindawi Publishing Corporationhttp://www.hindawi.com Volume 2014

Advances in

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Stem CellsInternational

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Enzyme Research

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International Journal of

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